Introduction
There are a variety of models utilized to evaluate behavior or categorize "why" behavior happens, develops, or changes.8 Veterinarians are trained to consider medical causes for behavior change; behavior is a symptom of a disease process to diagnose and treat. For example, an increase in aggressive behaviors (e.g., biting, lunging) may be due to pain or a brain tumor. Veterinarians also routinely consider ethological explanations for behavior. For example, an increase in aggressive behaviors may be due to elevated testosterone and territorial defense modal action patterns associated with breeding season.
In addition to these more familiar methods of behavior evaluation, applied behavior analysis (ABA) is critical to fully understand how behavior develops and is maintained in an individual animal.3,4,8 Behavior of individual animals will be influenced by past experiences (operant conditioning). Using the example above, increased aggressive behavior may be due to past reinforcement; the animal learned to do the behavior. The laws and rules that govern learning in individuals provide a robust method for examining behavior, evaluating and reducing problem behavior, and teaching specific behavior across species.2-4,7,8,14,19,23
These three models are not mutually exclusive. While it may seem obvious that animals can learn, this aspect of captive management is frequently overlooked when evaluating behavior. Many caretakers default only to the other models. For instance, if a monitor lizard lunges at a cage door and food is presented, lunging (or "attacking") will likely increase, as food will typically reinforce the behavior. However, the explanation for this type of behavior is generally that the animal or species is "aggressive" or "territorial." The more likely possibility that the animal learned to do the behavior in that context is generally not considered.
Principles of Applied Behavior Analysis
Behavior analysis applies to all species and investigates the universal laws of behavior change due to experience (i.e., learning). Applied behavior analysis (ABA) is the behavior change technology derived from behavior analysis and takes the individual animal's learning history and current environmental conditions into account and investigates the purpose (i.e., function) the behavior serves for the animal.
Behavior is not evaluated alone but instead always considered within the context of the environment immediately surrounding and functionally related to the behavior. Thus, the "smallest unit" of behavior is behavior (B) with the environmental brackets of the antecedent immediately before it (A) and the consequence (C) immediately after it (A-B- C).3,7,8 The observable behavior of interest is defined first, using clear, concise language to describe the relevant behavior. The consequence and antecedent are then identified and described. The ability to understand the functional relationship between a behavior and the environment immediately around it is critical when developing problem behavior response plans.7,8 This relationship between A-B-C is also the fundamental relationship developed when specific behaviors are purposefully trained.
Behavior is a function of its consequence (law of effect).3,7 A consequence is a stimulus, event, or condition that influences the strength of future behavior.3,7 Reinforcers are consequences that maintain or increase a behavior; punishers are those that decrease behavior. The consequence is defined by its effect on behavior.7 Consequences can also be categorized based on input: positive if added to the environment and negative if removed/escaped/avoided. Positive and negative are mathematical concepts; there is no connotation of "good/bad" in this context. There are four consequence options: positive reinforcement ("reward"), negative reinforcement ("escape"), positive punishment ("discipline/correction"), and negative punishment ("penalty/fine"). It is the learner who determines if something is reinforcement or punishment.7
The process of receiving feedback from the environment and feedback modifying future behavior (i.e., learning) is completely natural and happens constantly "in the wild" as well as "in captivity."3,7 While it may be used to purposefully train behavior, it is functioning at all times, not just in "training sessions." Every interaction caregivers have with their animals is a teaching opportunity. In addition, the animal's interactions with other animals and the overall environment will also provide constant feedback regarding the effectiveness of behavior.
There are predictable negative side effects to living in environments that are shifted toward negative reinforcement, positive punishment, and/or negative punishment compared to positive reinforcement.7 These include apathy/reduced activity, aggression, escape/avoidance, and over-generalized aversion to environment.7 Caregivers can use a better understanding of ABA to help create environments that increase the level of positive reinforcement available to animals in their care.
Detailed reviews of ABA are available for interested readers and online information regarding applied behavior analysis topics can be found at Dr. Susan Friedman's site http://behaviorworks.org.2-4,7,8,14
Use in Positive Reinforcement Training
Positive reinforcement training (PRT) is grounded in the science of ABA. Behaviors are deliberately trained by "adding" something to the environment immediately after a behavior. Based on understanding an individual animal and/or species, it is possible to predict the likely category of a consequence. Food is a reinforcer for many animals. But other stimuli can also be reinforcing, such as tactile stimuli (e.g., scratching the head) or access to a favorite toy or person. This can also be the source of inadvertently training undesirable behavior. As noted above, if a lunging at a door is followed by food/eating, it is predictable that lunging will increase. Undesirable behavior is often unintentionally trained this way.
When utilizing PRT, the full behavior is typically broken down into deliberate steps (successive approximations) from a current behavior to the final behavior.2,3,7,16,19,21 The current behavior may not look like the final behavior. There are technical aspects to providing effective reinforcement (e.g., developing shaping plans, delivering consequences with consistency and contiguity) that should be learned to improve trainer effectiveness.2,3,7,9,10,19,21
A variety of resources on PRT are available and can be extrapolated to other species.2-4,9,10,14,16,19,21,22 The online sites www.clickertraining.com and http://behaviorworks.org have examples in exotic species. The clickertraining.com site has excellent information on PRT in general. The Animal Behavior Management Alliance focuses on training and enrichment of all species and has an annual conference and a journal publication (Wellspring).
Training husbandry behaviors makes handling easier and safer. Training can facilitate basic management such as stationing in a specific part of the enclosure, voluntary blood draws, shifting from one enclosure to another, entering transportation crates, presenting feet for nail trim, coming when cued, holding still for a physical exam, and increasing activity.10,24 In addition, it is used in cognition research and higher level cognitive function has been shown in box turtles.15 In captive animal management, training and maintaining behavior with PRT increases the individual animal's behavioral repertoire, facilitates animal management, and creates greater opportunity for positive reinforcement.
While professional animal keepers are making great strides in utilizing deliberate training to facilitate care of a multitude of exotic species, many pet caregivers are unaware that their animals are capable of such learning. Presenting positive reinforcement training as a way to increase their bond with the animal and see more behavior from the animal can be motivating to many caregivers.
Use in Problem Behavior Reduction
Applied behavior analysis can be utilized to address problem behavior.2,6,7,10,13,19 Understanding and changing behavior results from identifying the discriminative stimuli that set the occasion for the behavior and the consequences that give the behavior strength. The focus of the behavior change plan is to modify the environment to set the occasion for appropriate alternative behaviors and reinforce them when they occur. The environment is modified to change the animal's behavior. Even complex, severe problem behavior is responsive to this approach.9,23
A functional assessment and intervention design (FAID) worksheet for evaluating problem behavior and developing appropriate behavior support plans is available.6 The FAID worksheet provides a standardized approach to cases and prompts a complete, individualized evaluation of the problem behavior situation and development of a plan specific to that individual in that environment.
Use in Enrichment
Deliberate environmental enrichment has increased in captive animal management.1,11,19,25 Positive reinforcement training can be considered environmental enrichment (cognitive stimulation).20 Other major categories of enrichment include habitat enrichment, sensory enrichment, manipulative enrichment, food enrichment (including hunting and foraging), and social groupings (when appropriate).
Understanding species natural history and sensory capabilities as well as the individual animal's learning history is important for developing appropriate enrichment goals. The Shape of Enrichment, Inc. (www.enrichment.org) is a leading animal enrichment organization with extensive online and printed resources. Ideas for reptile enrichment can also be found at www.reptilebehavior.com (VIN editor: as of 11-20-15 the link leads to a site with completely different topic).
The actual impact of the enrichment on the individual animal should be evaluated. If undesirable effects are seen (e.g., increased fighting, fear response), then the enrichment needs to be modified. Enrichment items or events should be varied over time to reduce habituation, which limits effectiveness. If animals are unaccustomed to exploring enrichment items, positive reinforcement training can be used to train interaction. In many cases, providing a minimally appropriate environment for reptiles is consistent with some level of environmental enrichment (e.g., thermal gradients and basking sites, hide/humidity boxes, soaking areas). Specific application of enrichment may lead to further health benefits (e.g., reducing obesity) and allow animals to more closely mimic natural behavioral repertoires and time budgets (e.g., foraging, climbing, hunting, digging).
Health effects of enrichment are typically studied using behavioral, physiologic, or neurologic models. Positive behavioral impacts include reduced aggression, reduced abnormal behavior, and increased normal behavior.1,11,18-20,22 Positive physiologic and neurologic effects include decreased cortisol levels, improved immune function, and improved cognitive function.5,12,13,17,20
Summary
Understanding applied behavior analysis can allow clinicians to more effectively work with caregivers to create environments conducive to improved reptile health and welfare.
References
1. Almli LM, Burghardt GM. Environmental enrichment alters the behavioral profile of ratsnakes (Elaphe). J Appl Anim Welf Sci. 2006;9:85–109.
2. Barlow-Irick P. How 2 Train a:__. Blanco, NM: Self-published; 2012.
3. Chance P. First Course in Applied Behavior Analysis. Long Grove, IL: Waveland Press; 2009.
4. Daniels AC. Other People's Habits. New York, NY: McGraw-Hill; 2001.
5. Fox C, Merali Z, Harrison C. Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav Brain Res. 2006;175:1–8.
6. Friedman SG. A framework for solving behavior problems: functional assessment and intervention design. J Exot Pet Med. 2007;16:6–10.
7. Friedman SG, Edling TM, Cheney CD. Concepts in behavior: Section I. In: Harrison GJ, Lightfoot TL, eds. Clinical Avian Medicine. Volume I. Palm Beach, FL: Spix Publishing; 2006: 46–59.
8. Friedman SG, Haug LI. From parrots to pigs to pythons: universal principles and procedures of learning. In: Tynes VV, ed. Behavior of Exotic Pets. Ames, IA: Wiley-Blackwell; 2010: 190–205.
9. Heidenreich B. The Parrot Problem Solver: Finding Solutions to Aggressive Behavior. Neptune City, NJ: T.F.H. Publications; 2005.
10. Hellmuth H, Augustine L, Watkins B, Hope K. Using operant condition and desensitization to facilitate veterinary care with captive reptiles. Vet Clin North Am Exot Anim Pract. 2012;15:424–443.
11. Hosey G, Melfi V, Pankhurst S. Environmental enrichment. In: Zoo Animals: Behavior, Management, and Welfare. Oxford, UK: Oxford University Press; 2009: 259–291.
12. Kotrschal A, Taborsky B. Environmental change enhances cognitive abilities in fish. PLoS Biol. 2010;8:e1000351. doi: 10.1371/journal.pbio.1000351.
13. Lambeth SP, Hau J, Perlman JE, Martino M, Schapiro SJ. Positive reinforcement training affects hematologic and serum chemistry values in captive chimpanzees (Pan troglodytes). Am J Primatol. 2006;68:245–256.
14. Latham GI. The Power of Positive Parenting. North Logan, UT: P&T Ink; 1990.
15. Leighty KH, Grand AP, Pittman CVL, Maloney MA, Bettinger TL. Relational responding by eastern box turtles (Terrapene carolina) in a series of color discrimination tasks. J Comp Psychol. 2013;127:256–264.
16. Miller P. The Power of Positive Dog Training. 2nd ed. Hoboken, NJ: Wiley Publishing, Inc.; 2008.
17. Morley-Fletcher S, Rea M, Maccari S, Laviola G. Environmental enrichment during adolescence reverses the effects of prenatal stress on play behavior and HPA axis reactivity in rats. Eur J Neurosci. 2003;18:3367–3374.
18. Novak MFSX, Kenney C, Suomi SJ, Ruppenthal GC. Use of animal-operated folding perches by rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci. 2007;46(6):35–43.
19. Pena Y, Prunell M, Rotllant D, Armario A, Escorihuela RM. Enduring effects of environmental enrichment from weaning to adulthood on pituitary-adrenal function, pre-pulse inhibition and learning in male and female rats. Psychoneuroendocrinology. 2009;34:1390–1404.
20. Pomerantz O, Terkel J. Effects of positive reinforcement training techniques on the psychological welfare of zoo-housed chimpanzees (Pan troglodytes). Am J Primatol. 2009;71:687–695.
21. Ramirez K. Animal Training: Successful Animal Management Through Positive Reinforcement. Chicago, IL: Shedd Aquarium; 1999.
22. Schapiro SJ, Bloomsmith MA, Laule GE. Positive reinforcement training as a technique to alter nonhuman primate behavior: quantitative assessments of effectiveness. J Appl Anim Welf Sci. 2003;6:175–187.
23. Susta F. Reducing aggressive behavior of kiang - Tibetan wild ass (Equus kiang hodereni) male in Prague Zoo. ABMA Wellspring. 2010;10,11:22–24.
24. Weiss E, Wilson S. The use of classical and operant condition in training Aldabra tortoises (Geochelone gigantea) for venipuncture and other husbandry issues. J Appl Anim Welf Sci. 2003;6:33–38.
25. Young RJ. Environmental Enrichment for Captive Animals. Herts, UK: Universities Federation for Animal Welfare; 2003.